The chromatin landscape of the euryarchaeon Haloferax volcanii

Abstract

Background Archaea, together with Bacteria, represent the two main divisions of life on Earth, with many of the defining characteristics of the more complex eukaryotes tracing their origin to evolutionary innovations first made in their archaeal ancestors. One of the most notable such features is nucleosomal chromatin, although archaeal histones and chromatin differ significantly from those of eukaryotes, not all archaea possess histones and it is not clear if histones are a main packaging component for all that do. Despite increased interest in archaeal chromatin in recent years, its properties have been little studied using genomic tools. Results Here, we adapt the ATAC-seq assay to archaea and use it to map the accessible landscape of the genome of the euryarchaeote Haloferax volcanii. We integrate the resulting datasets with genome-wide maps of active transcription and single-stranded DNA (ssDNA) and find that while H. volcanii promoters exist in a preferentially accessible state, unlike most eukaryotes, modulation of transcriptional activity is not associated with changes in promoter accessibility. Applying orthogonal single-molecule footprinting methods, we quantify the absolute levels of physical protection of H. volcanii and find that Haloferax chromatin is similarly or only slightly more accessible, in aggregate, than that of eukaryotes. We also evaluate the degree of coordination of transcription within archaeal operons and make the unexpected observation that some CRISPR arrays are associated with highly prevalent ssDNA structures. Conclusions Our results provide the first comprehensive maps of chromatin accessibility and active transcription in Haloferax across conditions and thus a foundation for future functional studies of archaeal chromatin.

Interplay of intracellular and trans‐cellular DNA methylation in natural archaeal consortia

“…The integrity of the partially methylated genome can only be maintained if the ability of the cognate REases to bind DNA with alternative GC content is also reduced, considerably diminishing the effectiveness of the RM systems in protecting the host from viruses and conjugative plasmids. The observed inaccessibility of DNA loci with alternative GC compositions to MTases agrees with the published report that the Haloferax volcanii chromatin with alternative GC composition is generally less accessible to DNA binding proteins (Marinov et al, 2023 ). Apparently, for inhabitants of extreme environments, such as many archaea, the possibility of lateral gene exchange is as important for their survival as protection from allochthonous DNA (Wang et al, 2023 ).…”

“…First, representatives of this genus are widely recognized as model organisms, including for the study of archaeal methylomics. Different RM systems have been reported in different Haloferax species (Aguirre Sourrouille et al, 2022;DasSarma et al, 2019;Harris & Goldman, 2020;Marinov et al, 2023;Ouellette et al, 2018;Ouellette et al, 2020;Pérez-Arnaiz et al, 2020). The most common in Haloferax is the Mrr-RM system, found in the genomes of multiple Haloferax species.…”

“…Like many other Haloferax species, the H. lucertense SVX82 strain contains three plasmids, which made it possible to synchronously compare patterns of chromosome and plasmid methylation in this archaeon. The functional significance of DNA methylation can be gleaned from the distribution of methylated sites in both coding and non‐coding regions, as well as in regions proximal to the transcription start sites (TSSs) (Couturier & Lindås, 2018 ; Marinov et al, 2023 ). In this study, we used several statistical approaches to analyse the distribution of methylated sites and unmethylated canonical motifs in the protein‐coding regions, in the 75 bp‐long TSS upstream regions, and non‐coding sequences of the H. lucertense SVX82 genome.…”